Results

The fusiform cell dendritic arbors were quantified by a series of
measurements inspired by the work of Blackstad et al.
(1984)in the cat and described fully in METHODS.
The results serve asa basis for comparison of the gerbil to the cat
and as a basisfor a subsequent quantitative examination of the
relationshipbetween physiology and anatomy. It is important to note
that Blackstadet al. limited their consideration to the central third
of theDCN and thus avoided effects due to the significant curvatureof
the nucleus at its edges. It was not possible to do likewisein our
case due to the sample size limitations inherent to anin vivo
intracellular survey of thiskind.

The anatomical properties of the apical arbors are summarized in Table
1. Estimates were made of the total
dendritic lengthsby summing the lengths of the individual segments
comprising eachthree-dimensional (3-D) reconstruction. The mean apical
lengthwas 3,359 µm, which is very close to the mean value of 3,212 µmreported by Blackstad et al. (1984) in the cat. The
width andthickness measurements were obtained by rotating the arbor
aboutits long axis to find the widest and narrowest projections,
respectively.Both measures are smaller in the gerbil than in the cat,
althoughthe ratio, which reflects the degree of arbor planarity, is
approximatelythe same in both cases (2.56 in the gerbil, roughly 3 in
the cat).The mean height of the apical arbor, measured parallel to thelong axis, was 157 µm in the gerbil as compared with 267 µm inthe
cat.

Table 2 lists the anatomical properties
of the basal dendrites in this study. The mean total length was 1,925 µm, as comparedwith 2,728 µm in the cat. The mean arbor width is
smaller in thegerbil (314 µm) than in the cat (392 µm), but the
thickness islarger (112 vs. 72 µm). The result is that the width to
thicknessratio in the gerbil (3.07) is about half that in the cat
(5.70).The mean basal arbor is 250 µm in height as compared with 389µm in the cat.

Tonotopy

A qualitative illustration of the tonotopic organization is
presented in Fig. 2A, in which
the 17 fusiform cells of this studyhave been mapped onto a single DCN.
Only the basal dendrites havebeen drawn because that is presumably
where fusiform cells receiveacoustic input (Smith and Rhode
1985). The dendrites are colorcoded according to BF, as shown.
Figure 2A qualitatively suggeststhat the gerbil DCN has a
substantial volume devoted to relativelow BFs. The orderly arrangement
of cells by BF is also apparent,with the lowest BFs in the
rostral-most and ventrolateral-mostaspect of the nucleus.

Figure 2A shows that BF increases in both the dorsomedial
and caudal directions. This observation is quantified in Fig.
2Bwhere the BF is plotted as a function of the relative
X-positions(ventrolateral-to-dorsomedial location) and the
relative Z-positions(rostral-to-caudal location) of the
fusiform cell somata. Thestraight line fits to these data indicate
that BF is indeed highlycorrelated with these twodimensions.

The tonotopic axis is described by the equation log(BF) = 1.45Px + 1.01Pz (r = 0.81, P < 0.001), obtained by performing multiplelinear
regression on log BF using both the relative X- and
Z-positions.A tonotopic position was determined for each
neuron by projectingits location onto this axis and computing the
distance from theorigin (Px = Pz = 0).
The resulting positions are plotted in Fig.3 as a function of BF. For comparison,
the place-frequency mapfor the gerbil cochlea is also plotted, where
position indicatesthe relative distance from the base of the cochlea.
In general,Fig. 3 shows that the spatial distribution of BFs in the
DCN closelyfollows the distribution of characteristic frequencies
(CFs) alongthe cochlea. For comparison, the place-frequency map
computedfor the cat DCN by Spirou et al. (1993) is also
plotted.

Fusiform cell orientation varies with location

Figure 4 summarizes a systematic
shift in the orientation of the long axis as a function of
rostral-caudal position. In therostral end of the nucleus, the apical
dendrites tend to be positionedon the rostral side of the soma while
the basal dendrites extendin the caudal direction. Near the center of
the DCN, the orientationis roughly vertical (dorsal to ventral).
Toward the caudal pole,fusiform cells have caudally directed apical
dendrites and rostrallydirected basal dendrites.

It would appear that this trend is a consequence of the shape of the
DCN itself. The DCN can be visualized as a series ofthin shells, with
the molecular layer wrapped around the fusiformcell layer, which in
turn is wrapped around the deep layer. Thusfrom any position within
the fusiform cell layer, the apical dendritesradiate outward to fill
the molecular layer while the basal dendritesconverge inward to occupy
the deep layer. A similar finding wasreported by Rhode et al.
(1983), who further describe the cellsin the rostral end
having more numerous apical dendrites thatmore frequently emerge
directly from the soma. Neither this studynor the previous one finds
any obvious physiological sequellaeto this trend, which possibly is
simply a consequence of the overallcurvature of thenucleus.

Spontaneous rate depends on basal dendrite orientation

The spontaneous discharge rates of the fusiform cells in this
sample range from 0 to 54 spikes/s. These can be separated intoa low
SR group (rate <2.5 spikes/s, 8/17 cells) and a high SRgroup (rate
>7.5 spikes/s, 9/17 cells). The creation of two SRcategories may, in
fact, represent an artificial division of acontinuously distributed
property, but is useful here as a convenientmeans of visualizing a
related anatomical trend. Specifically,there is a correlation between
spontaneous rate group and thedisposition of the basal dendrites, as
depicted in Fig. 5. Thebasal dendrites
of the low SR cells (top row) are primarily directedcaudally away from the soma. The high SR cells (bottom row)
tendalso to have branches oriented in the rostral direction, givingthe distribution of the basal dendrites a more symmetrical appearance.

These observations were put on a more quantitative basis by computing
the centroid of each basal arbor with respect to thesoma. The trend is
specifically captured by the rostral-caudalcomponent,
ZC, as shown in Fig. 5. Note that the
value of ZC ispositive for positions
caudal to the soma. For every low SR cell(ZC 63.2 µm), the basal arbor
centroid is caudal to that ofevery high SR cell
(ZC 48.8 µm). No correlation was
found betweenthe absolute position of the basal arbor centroid and
spontaneousactivity.

The nine cells shown in Fig. 5 come from the same general region of the
DCN, reflected by the similarity of their best frequencies.This is an
important consideration when examining the arrangementof the basal
dendrites, because as described above, the orientationof the fusiform
cell long axis changes as a function of position(Fig. 4).

Input resistance is a function of total apical dendritic length

Figure 6 shows that fusiform cell
input resistance is correlated with apical dendritic length, but not
with basal dendriticlength. The best line fit to the apical length was
computed afterremoving the two points indicated by triangles in Fig.
6A. Thecorrelation with apical length is negative, so that
larger lengthscorrespond to smaller resistances. This is consistent
with a passivemodel in which membrane conductance is proportional to
surfacearea, insofar as dendritic surface area is proportional to
totallength. Input resistance was not correlated with the sum of theapical and basal lengths (r = 0.06). The presence of
spines,however, greatly increases the surface area per unit length ofthe apical dendrite and so a simple sum of total lengths probablyunderstates the contribution of the apical dendrite to the
overallpassive membrane conductance. We did not consider the effectsof surface area more directly because of difficulties estimatingit
that arose from inconsistencies in the quality of spine labeling.

Regularity histogram shape depends on orientation of apical
arbor

Regularity histogram shapes were quantified using three slope
measurements as described in the companion paper. Briefly, thetransient slope, mT, most closely
follows the classification schemeof Gdowski (1995). It
is particularly sensitive to the changein interspike interval over the
initial 5-10 ms of response andsince nearly all of the cells in this
study had decreasing intervalsover this range, regardless of their
subsequent behavior, thetransient slope was not necessarily an
effective means of characterizingrate trends over the entire stimulus
duration. To better capturethese rate trends, the slope measurements
m1 and
m2 were computedby performing a
two-line fit to the interspike interval data afteromitting the
firstbin.

Figure 7 shows that for the 10 fusiform
cells with BFs less than 2 kHz, the slope
m1 is correlated with the orientation
ofthe apical dendrites. The angle apical
corresponds to the rotationrequired to find the narrowest dendritic
profile after makingthe long axis of the arbor vertical. A value of
zero correspondsto an arbor oriented perpendicular to the coronal
plane. The apicaldendrites in Fig. 7 are drawn looking down on their
tops, suchthat their long axes project out of the page. The values of
m1have been divided into three
groups: high, medium, and low, indicatedin Fig. 7 by circles,
triangles, and squares, respectively. Thedata indicate that the
fusiform cells with apical arbors orientedmost nearly perpendicular to
the coronal plane have the most positivem1 values (circles), while those
oriented closest to parallelto the coronal plane have the most
negative m1 values (squares).

Correlation of cell properties with location

An effort was made to identify fusiform cell characteristics that
vary systematically with location. To do this, a wide varietyof
physiological response metrics (see companion paper) were
systematicallycorrelated with the normalized X-,
Y-, and Z-position measurements(see
METHODS).

Two statistically significant trends were identified, roughly
orthogonal to the tonotopic axis. The relative noise index decreasedin
the X-direction (ventrolateral to dorsomedial), meaning thatthe responses to noise became progressively weaker in this direction(Fig. 8A). A gradient in
wideband inhibitory strength is sufficientto account for this
observation, as detailed in the DISCUSSION.The second
trend was that input resistance also tended to decreasein the
X-direction (Fig. 8B). This is consistent with
the factthat total apical dendritic length increases in the same
direction(Fig. 8C), since the inverse relationship between
these two propertieshas already been described.

Aside from tonotopy, the only statistically significant spatial trends
were found in the X-direction. Since neither trendwas
accompanied by a significant dependence on Z-position, itwas not possible to compute an axis trajectory for quantitativecomparison with the tonotopic axis computed above. It can, however,be
said that while best frequency is strongly correlated withboth
X- and Z-position, input resistance and relative
noise responseare strongly correlated only with X-position.
So, although theseresults cannot resolve the issue of an orthogonal
axis per se,there is at least a qualitative suggestion that the
spatial gradientsof these two properties are not parallel with the
frequencyaxis.